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Dark rearing reveals the mechanism underlying stimulus size tuning of superior colliculus neurons

Published online by Cambridge University Press:  04 October 2006

KHALEEL A. RAZAK
Affiliation:
Graduate Program in Neurobiology and Behavior, Department of Biology, Georgia State University, Atlanta, Georgia Current address for Khaleel Razak: Department of Zoology and Physiology, Biological Science Bldg. 410, University of Wyoming, Laramie, WY 82071
SARAH L. PALLAS
Affiliation:
Graduate Program in Neurobiology and Behavior, Department of Biology, Georgia State University, Atlanta, Georgia

Abstract

Neurons in the superficial layers of the midbrain superior colliculus (SC) exhibit distinct tuning properties for visual stimuli, but, unlike neurons in the geniculocortical visual pathway, most respond best to visual stimuli that are smaller than the classical receptive field (RF). The mechanism underlying this size selectivity may depend on the number and pattern of feedforward retinal inputs and/or the balance between inhibition and excitation within the RF. We have previously shown that chronic blockade of NMDA receptors (NMDA-R), which increases the convergence of retinal afferents onto SC neurons, does not alter size selectivity in the SC. This suggests that the number of retinal inputs does not determine size selectivity. Here we show, using single unit extracellular recordings from the SC of normal hamsters, that size selectivity in neurons selective for small stimulus size is correlated with the strength of inhibition within the RF. We also show that dark rearing causes concomitant reductions in both inhibition and size selectivity. In addition, dark rearing increases the percentage of neurons non-selective for stimulus size. Finally, we show that chronic blockade of NMDA-R, a procedure that does not alter size tuning, also does not change the strength of inhibition within the RF. Taken together, these results argue that inhibition within the RF underlies selectivity for small stimulus size and that inhibition must be intact for size tuning to be preserved after developmental manipulations of activity. In addition, these results suggest that regulation of the balance between excitation and inhibition within the RF does not require NMDA-R activity but does depend on visual experience. These results suggest that developmental experience influences neural response properties through an alteration of inhibitory circuitry.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477504.CrossRefGoogle Scholar
Benevento, L.A., Bakkum, B.W., Port, J.D., & Cohen, R.S. (1992). The effects of dark-rearing on the electrophysiology of the rat visual cortex. Brain Research 572, 198207.CrossRefGoogle Scholar
Betts, L.R., Taylor, C.P., Sekuler, A.B., & Bennett, P.J. (2005). Aging reduces center-surround antagonism in visual motion processing. Neuron 45, 361366.CrossRefGoogle Scholar
Binns, K.E. & Salt, T.E. (1997). Different roles for GABA-A and GABA-B receptors in visual processing in the rat superior colliculus. Journal of Physiology 504, 629639.CrossRefGoogle Scholar
Binns, K.E. & Salt, T.E. (1998). Developmental changes in NMDA receptor-mediated visual activity in the rat superior colliculus, and the effect of dark rearing. Experimental Brain Research 120, 335344.CrossRefGoogle Scholar
Carrasco, M.M. & Pallas, S.L. (2006). Early visual experience prevents but cannot reverse deprivation-induced loss of refinement in adult superior colliculus. Visual Neuroscience (In press).CrossRefGoogle Scholar
Carrasco, M.M., Razak, K.A., & Pallas, S.L. (2005). Visual experience is necessary for maintenance but not development of receptive fields in superior colliculus. Journal of Neurophysiology 94, 19621970.CrossRefGoogle Scholar
Chen, L., Cooper, N.G., & Mower, G.D. (2000). Developmental changes in the expression of NMDA receptor subunits (NR1, NR2A, NR2B) in the cat visual cortex and the effects of dark rearing. Brain Research: Molecular Brain Research 78, 196200.CrossRefGoogle Scholar
Chen, L., Yang, C., & Mower, G.D. (2001). Developmental changes in the expression of GABA(A) receptor subunits (alpha[1], alpha[2], alpha[3]) in the cat visual cortex and the effects of dark rearing. Brain Research: Molecular Brain Research 88, 135143.CrossRefGoogle Scholar
Czepita, D., Reid, S.N., & Daw, N.W. (1994). Effect of longer periods of dark rearing on NMDA receptors in cat visual cortex. Journal of Neurophysiology 72, 12201226.Google Scholar
Eysel, U.T., Shevelev, I.A., & Sharaev, G.A. (1998). Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition. Neuroscience 84, 2536.CrossRefGoogle Scholar
Foeller, E. & Feldman, D.E. (2004). Synaptic basis for developmental plasticity in somatosensory cortex. Current Opinion in Neurobiology 14, 8995.CrossRefGoogle Scholar
Fox, K., Daw, N., Sato, H., & Czepita, D. (1991). Dark-rearing delays the loss of NMDA-receptor function in kitten visual cortex. Nature 350, 342344.CrossRefGoogle Scholar
Gianfranceschi, L., Siciliano, R., Walls, J., Morales, B., Kirkwood, A., Huang, Z.J., Tonegawa, S., & Maffei, L. (2003). Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proceedings of the National Academy of Sciences of the United States of America 100, 1248612491.CrossRefGoogle Scholar
Goodwin, A.W. & Henry, G.H. (1978). The influence of stimulus velocity on the responses of single neurones in the striate cortex. Journal of Physiology 277, 467482.CrossRefGoogle Scholar
Gordon, B., Kinch, G., Kato, N., Keele, C., Lissman, T., & Fu, L.N. (1997). Development of MK-801, kainate, AMPA, and muscimol binding sites and the effect of dark rearing in rat visual cortex. Journal of Comparative Neurology 383, 7381.3.0.CO;2-I>CrossRefGoogle Scholar
Grubb, M.S. & Thompson, I.D. (2004). The influence of early experience on the development of sensory systems. Current Opinion in Neurobiology 14, 503512.CrossRefGoogle Scholar
Hensch, T.K. (2004). Critical period regulation. Annu Rev Neurosci 27, 549579.CrossRefGoogle Scholar
Hensch, T.K. & Fagiolini, M. (2005). Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Progress in Brain Research 147, 115124.CrossRefGoogle Scholar
Hua, T., Li, X., He, L., Zhou, Y., Wang, Y., & Leventhal, A.G. (2006). Functional degradation of visual cortical cells in old cats. Neurobiology of Aging 27, 155162.CrossRefGoogle Scholar
Huang, L. & Pallas, S.L. (2001). NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression. Journal of Neurophysiology 86, 11791194.Google Scholar
Humphrey, A.L. & Saul, A.B. (1998). Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. Journal of Neurophysiology 80, 29913004.Google Scholar
Itaya, S.K., Fortin, S., & Molotchnikoff, S. (1995). Evolution of spontaneous activity in the developing rat superior colliculus. Canadian Journal of Physiology and Pharmacology 73, 13721377.CrossRefGoogle Scholar
Leventhal, A.G., Wang, Y., Pu, M., Zhou, Y., & Ma, Y. (2003). GABA and its agonists improved visual cortical function in senescent monkeys. Science 300, 812815.CrossRefGoogle Scholar
Maggi, C.A. & Meli, A. (1986). Suitability of urethane anesthesia for physiopharmacological investigations. Part 3: Other systems and conclusions. Experientia 42, 531537.Google Scholar
Morales, B., Choi, S.Y., & Kirkwood, A. (2002). Dark rearing alters the development of GABAergic transmission in visual cortex. Journal of Neuroscience 22, 80848090.Google Scholar
Murata, A., Gallese, V., Luppino, G., Kaseda, M., & Sakata, H. (2000). Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. Journal of Neurophysiology 83, 25802601.Google Scholar
Murthy, A. & Humphrey, A.L. (1999). Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17. Journal of Neurophysiology 81, 121224.Google Scholar
Pallas, S.L., Xu, M., & Razak, K.A. (2006). Influence of thalamocortical activity on sensory cortical development and plasticity. In Development and Plasticity in Sensory Thalamus and Cortex, eds. R. Erzurumlu, W. Guido & Z. Molnar. New York: Kluwer Academic/Plenum Publishers.
Pallas, S.L. & Finlay, B.L. (1989). Conservation of receptive field properties of superior colliculus cells after developmental rearrangements of retinal input. Visual Neuroscience 2, 121135.CrossRefGoogle Scholar
Patel, H.H. & Sillito, A.M. (1978). Inhibition and velocity tuning in the cat visual cortex (Proceedings). Journal of Physiology 284, 113114.Google Scholar
Rajan, R. (1998). Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nature Neuroscience 1, 138143.CrossRefGoogle Scholar
Razak, K.A., Huang, L., & Pallas, S.L. (2003). NMDA receptor blockade in the superior colliculus increases receptive field size without altering velocity and size tuning. Journal of Neurophysiology 90, 110119.CrossRefGoogle Scholar
Razak, K.A. & Pallas, S.L. (2005). Neural mechanisms of stimulus velocity tuning in the superior colliculus. Journal of Neurophysiology 94, 35733589.CrossRefGoogle Scholar
Rhoades, R.W. & Chalupa, L.M. (1978). Functional properties of the corticotectal projection in the golden hamster. Journal of Comparative Neurology 180, 617634.CrossRefGoogle Scholar
Ruthazer, E.S. (2005). You're perfect, now change-redefining the role of developmental plasticity. Neuron 45, 825828.CrossRefGoogle Scholar
Schliebs, R., Rothe, T., & Big, L.V. (1986). Dark-rearing affects the development of benzodiazepine receptors in the central visual structures of rat brain. Brain Research 389, 179185.CrossRefGoogle Scholar
Shapley, R., Hawken, M., & Ringach, D.L. (2003). Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38, 689699.CrossRefGoogle Scholar
Sillito, A.M. (1975). The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. Journal of Physiology (London) 250, 305329.CrossRefGoogle Scholar
Stein, B.E. & Dixon, J.P. (1979). Properties of superior colliculus neurons in the golden hamster. Journal of Comparative Neurology 183, 269284.CrossRefGoogle Scholar
Tongiorgi, E., Ferrero, F., Cattaneo, A., & Domenici, L. (2003). Dark-rearing decreases NR2A N-methyl-D-aspartate receptor subunit in all visual cortical layers. Neuroscience 119, 10131022.CrossRefGoogle Scholar
Vale, C., Schoorlemmer, J., & Sanes, D.H. (2003). Deafness disrupts chloride transporter function and inhibitory synaptic transmission. Journal of Neuroscience 23, 75167524.Google Scholar
Vaney, D.I. & Taylor, W.R. (2002). Direction selectivity in the retina. Current Opinion in Neurobiology 12, 405410.CrossRefGoogle Scholar
Zheng, W. & Knudsen, E.I. (1999). Functional selection of adaptive auditory space map by GABAA-mediated inhibition. Science 284, 962965.CrossRefGoogle Scholar